Isp7 Is a Novel Regulator of Amino Acid Uptake in the TOR Signaling Pathway

REFERENCES

• Soulard A, Cohen A, Hall MN. 2009. TOR signaling in invertebrates. Curr. Opin. Cell Biol. 21:825–836. http://dx.doi.org/10.1016/j.ceb.2009.08.007.
   PubMed Web of Science ®Google Scholar
• Zoncu R, Efeyan A, Sabatini DM. 2011. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 12:21–35. http://dx.doi.org/10.1038/nrm3025.
   PubMed Web of Science ®Google Scholar
• Heitman J, Movva NR, Hall MN. 1991. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253:905–909. http://dx.doi.org/10.1126/science.1715094.
   PubMed Web of Science ®Google Scholar
• Loewith R, Jacinto E, Wullschleger S, Lorberg A, Crespo JL, Bonenfant D, Oppliger W, Jenoe P, Hall MN. 2002. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10:457–468. http://dx.doi.org/10.1016/S1097-2765(02)00636-6.
   PubMed Web of Science ®Google Scholar
• Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. 2004. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 14:1296–1302. http://dx.doi.org/10.1016/j.cub.2004.06.054.
   PubMed Web of Science ®Google Scholar
• Lamming DW, Ye L, Katajisto P, Goncalves MD, Saitoh M, Stevens DM, Davis JG, Salmon AB, Richardson A, Ahima RS, Guertin DA, Sabatini DM, Baur JA. 2012. Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science 335:1638–1643. http://dx.doi.org/10.1126/science.1215135.
   PubMed Web of Science ®Google Scholar
• Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM. 2006. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22:159–168. http://dx.doi.org/10.1016/j.molcel.2006.03.029.
   PubMed Web of Science ®Google Scholar
• Astrinidis A, Henske EP. 2005. Tuberous sclerosis complex: linking growth and energy signaling pathways with human disease. Oncogene 24:7475–7481. http://dx.doi.org/10.1038/sj.onc.1209090.
   PubMedGoogle Scholar
• Kwiatkowski DJ, Manning BD. 2005. Tuberous sclerosis: a GAP at the crossroads of multiple signaling pathways. Hum. Mol. Genet. 14:R251–R258. http://dx.doi.org/10.1093/hmg/ddi260.
   PubMed Web of Science ®Google Scholar
• Long X, Lin Y, Ortiz-Vega S, Yonezawa K, Avruch J. 2005. Rheb binds and regulates the mTOR kinase. Curr. Biol. 15:702–713. http://dx.doi.org/10.1016/j.cub.2005.02.053.
   PubMed Web of Science ®Google Scholar
• Smith EM, Finn SG, Tee AR, Browne GJ, Proud CG. 2005. The tuberous sclerosis protein TSC2 is not required for the regulation of the mammalian target of rapamycin by amino acids and certain cellular stresses. J. Biol. Chem. 280:18717–18727. http://dx.doi.org/10.1074/jbc.M414499200.
   PubMed Web of Science ®Google Scholar
• Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, Sabatini DM. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320:1496–1501. http://dx.doi.org/10.1126/science.1157535.
   PubMed Web of Science ®Google Scholar
• Weisman R, Choder M. 2001. The fission yeast TOR homolog, tor1+, is required for the response to starvation and other stresses via a conserved serine. J. Biol. Chem. 276:7027–7032. http://dx.doi.org/10.1074/jbc.M010446200.
   PubMed Web of Science ®Google Scholar
• Hayashi T, Hatanaka M, Nagao K, Nakaseko Y, Kanoh J, Kokubu A, Ebe M, Yanagida M. 2007. Rapamycin sensitivity of the Schizosaccharomyces pombe tor2 mutant and organization of two highly phosphorylated TOR complexes by specific and common subunits. Genes Cells 12:1357–1370. http://dx.doi.org/10.1111/j.1365-2443.2007.01141.x.
   PubMed Web of Science ®Google Scholar
• Ikai N, Nakazawa N, Hayashi T, Yanagida M. 2011. The reverse, but coordinated, roles of Tor2 (TORC1) and Tor1 (TORC2) kinases for growth, cell cycle and separase-mediated mitosis in Schizosaccharomyces pombe. Open Biol. 1:110007. http://dx.doi.org/10.1098/rsob.110007.
   PubMedGoogle Scholar
• Kawai M, Nakashima A, Ueno M, Ushimaru T, Aiba K, Doi H, Uritani M. 2001. Fission yeast tor1 functions in response to various stresses including nitrogen starvation, high osmolarity, and high temperature. Curr. Genet. 39:166-174. http://dx.doi.org/10.1007/s002940100198.
   PubMed Web of Science ®Google Scholar
• Matsuo T, Otsubo Y, Urano J, Tamanoi F, Yamamoto M. 2007. Loss of the TOR kinase Tor2 mimics nitrogen starvation and activates the sexual development pathway in fission yeast. Mol. Cell. Biol. 27:3154–3164. http://dx.doi.org/10.1128/MCB.01039-06.
   PubMed Web of Science ®Google Scholar
• Petersen J, Nurse P. 2007. TOR signalling regulates mitotic commitment through the stress MAP kinase pathway and the Polo and Cdc2 kinases. Nat. Cell Biol. 9:1263–1272. http://dx.doi.org/10.1038/ncb1646.
   PubMed Web of Science ®Google Scholar
• Schonbrun M, Laor D, Lopez-Maury L, Bahler J, Kupiec M, Weisman R. 2009. TOR complex 2 controls gene silencing, telomere length maintenance, and survival under DNA-damaging conditions. Mol. Cell. Biol. 29:4584–4594. http://dx.doi.org/10.1128/MCB.01879-08.
   PubMedGoogle Scholar
• Weisman R, Roitburg I, Nahari T, Kupiec M. 2005. Regulation of leucine uptake by tor1+ in Schizosaccharomyces pombe is sensitive to rapamycin. Genetics 169:539–550. http://dx.doi.org/10.1534/genetics.104.034983.
   PubMedGoogle Scholar
• Alvarez B, Moreno S. 2006. Fission yeast Tor2 promotes cell growth and represses cell differentiation. J. Cell Sci. 119:4475–4485. http://dx.doi.org/10.1242/jcs.03241.
   PubMed Web of Science ®Google Scholar
• Uritani M, Hidaka H, Hotta Y, Ueno M, Ushimaru T, Toda T. 2006. Fission yeast Tor2 links nitrogen signals to cell proliferation and acts downstream of the Rheb GTPase. Genes Cells 11:1367–1379. http://dx.doi.org/10.1111/j.1365-2443.2006.01025.x.
   PubMed Web of Science ®Google Scholar
• Valbuena N, Guan KL, Moreno S. 2012. The Vam6 and Gtr1-Gtr2 pathway activates TORC1 in response to amino acids in fission yeast. J. Cell Sci. 125:1920–1928. http://dx.doi.org/10.1242/jcs.094219.
   PubMedGoogle Scholar
• Weisman R, Finkelstein S, Choder M. 2001. Rapamycin blocks sexual development in fission yeast through inhibition of the cellular function of an FKBP12 homolog. J. Biol. Chem. 276:24736–24742. http://dx.doi.org/10.1074/jbc.M102090200.
   PubMedGoogle Scholar
• Weisman R, Roitburg I, Schonbrun M, Harari R, Kupiec M. 2007. Opposite effects of tor1 and tor2 on nitrogen starvation responses in fission yeast. Genetics 175:1153–1162. http://dx.doi.org/10.1534/genetics.106.064170.
   PubMed Web of Science ®Google Scholar
• Urano J, Comiso MJ, Guo L, Aspuria PJ, Deniskin R, Tabancay APJr, Kato-Stankiewicz J, Tamanoi F. 2005. Identification of novel single amino acid changes that result in hyperactivation of the unique GTPase, Rheb, in fission yeast. Mol. Microbiol. 58:1074–1086. http://dx.doi.org/10.1111/j.1365-2958.2005.04877.x.
   PubMedGoogle Scholar
• Urano J, Sato T, Matsuo T, Otsubo Y, Yamamoto M, Tamanoi F. 2007. Point mutations in TOR confer Rheb-independent growth in fission yeast and nutrient-independent mammalian TOR signaling in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 104:3514–3519. http://dx.doi.org/10.1073/pnas.0608510104.
   PubMed Web of Science ®Google Scholar
• van Slegtenhorst M, Mustafa A, Henske EP. 2005. Pas1, a G1 cyclin, regulates amino acid uptake and rescues a delay in G1 arrest in Tsc1 and Tsc2 mutants in Schizosaccharomyces pombe. Hum. Mol. Genet. 14:2851–2858. http://dx.doi.org/10.1093/hmg/ddi317.
   PubMedGoogle Scholar
• Matsumoto S, Bandyopadhyay A, Kwiatkowski DJ, Maitra U, Matsumoto T. 2002. Role of the Tsc1-Tsc2 complex in signaling and transport across the cell membrane in the fission yeast Schizosaccharomyces pombe. Genetics 161:1053–1063. http://www.genetics.org/content/161/3/1053.full.pdf.
   PubMedGoogle Scholar
• van Slegtenhorst M, Carr E, Stoyanova R, Kruger W, Henske EP. 2004. Tsc1+ and tsc2+ regulate arginine uptake and metabolism in Schizosaccharomyces pombe. J. Biol. Chem. 279:12706–12713. http://dx.doi.org/10.1074/jbc.M313874200.
   PubMed Web of Science ®Google Scholar
• Matsuo T, Kubo Y, Watanabe Y, Yamamoto M. 2003. Schizosaccharomyces pombe AGC family kinase Gad8p forms a conserved signaling module with TOR and PDK1-like kinases. EMBO J. 22:3073–3083. http://dx.doi.org/10.1093/emboj/cdg298.
   PubMed Web of Science ®Google Scholar
• Rallis C, Codlin S, Bahler J. 2013. TORC1 signaling inhibition by rapamycin and caffeine affect lifespan, global gene expression and cell proliferation of fission yeast. Aging Cell 12:563–573. http://dx.doi.org/10.1111/acel.12080.
   PubMed Web of Science ®Google Scholar
• Nakashima A, Otsubo Y, Yamashita A, Sato T, Yamamoto M, Tamanoi F. 2012. Psk1, an AGC kinase family member in fission yeast, is directly phosphorylated and controlled by TORC1 and functions as S6 kinase. J. Cell Sci. 125:5840–5849. http://dx.doi.org/10.1242/jcs.111146.
   PubMed Web of Science ®Google Scholar
• Takahara T, Maeda T. 2012. TORC1 of fission yeast is rapamycin-sensitive. Genes Cells 17:698–708. http://dx.doi.org/10.1111/j.1365-2443.2012.01618.x.
   PubMed Web of Science ®Google Scholar
• Weisman R, Choder M, Koltin Y. 1997. Rapamycin specifically interferes with the developmental response of fission yeast to starvation. J. Bacteriol. 179:6325–6334.
   PubMedGoogle Scholar
• Moreno S, Klar A, Nurse P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795–823. http://dx.doi.org/10.1016/0076-6879(91)94059-L.
   PubMed Web of Science ®Google Scholar
• Maundrell K. 1993. Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123:127–130. http://dx.doi.org/10.1016/0378-1119(93)90551-D.
   PubMed Web of Science ®Google Scholar
• Longtine MS, McKenzie AIII, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953–961.
   PubMed Web of Science ®Google Scholar
• Lafuente MJ, Petit T, Gancedo C. 1997. A series of vectors to construct lacZ fusions for the study of gene expression in Schizosaccharomyces pombe. FEBS Lett. 420:39–42. http://dx.doi.org/10.1016/S0014-5793(97)01486-5.
   PubMedGoogle Scholar
• Rose M, Botstein D. 1983. Construction and use of gene fusions to lacZ (beta-galactosidase) that are expressed in yeast. Methods Enzymol. 101:167–180. http://dx.doi.org/10.1016/0076-6879(83)01012-5.
   PubMed Web of Science ®Google Scholar
• Sato S, Suzuki H, Widyastuti U, Hotta Y, Tabata S. 1994. Identification and characterization of genes induced during sexual differentiation in Schizosaccharomyces pombe. Curr. Genet. 26:31–37. http://dx.doi.org/10.1007/BF00326301.
   PubMedGoogle Scholar
• Shimanuki M, Chung SY, Chikashige Y, Kawasaki Y, Uehara L, Tsutsumi C, Hatanaka M, Hiraoka Y, Nagao K, Yanagida M. 2007. Two-step, extensive alterations in the transcriptome from G0 arrest to cell division in Schizosaccharomyces pombe. Genes Cells 12:677–692. http://dx.doi.org/10.1111/j.1365-2443.2007.01079.x.
   PubMedGoogle Scholar
• Mata J, Lyne R, Burns G, Bahler J. 2002. The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 32:143–147. http://dx.doi.org/10.1038/ng951.
   PubMed Web of Science ®Google Scholar
• Valbuena N, Moreno S. 2010. TOR and PKA pathways synergize at the level of the Ste11 transcription factor to prevent mating and meiosis in fission yeast. PLoS One 5:e11514. http://dx.doi.org/10.1371/journal.pone.0011514.
   PubMedGoogle Scholar
• Kaufmann I, White E, Azad A, Marguerat S, Bahler J, Proudfoot NJ. 2010. Transcriptional activation of the general amino acid permease gene per1 by the histone deacetylase Clr6 is regulated by Oca2 kinase. Mol. Cell. Biol. 30:3396–3410. http://dx.doi.org/10.1128/MCB.00971-09.
   PubMedGoogle Scholar
• Aspuria PJ, Tamanoi F. 2008. The Tsc/Rheb signaling pathway controls basic amino acid uptake via the Cat1 permease in fission yeast. Mol. Genet. Genomics 279:441–450. http://dx.doi.org/10.1007/s00438-008-0320-y.
   PubMedGoogle Scholar
• Beck T, Schmidt A, Hall MN. 1999. Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J. Cell Biol. 146:1227–1238. http://dx.doi.org/10.1083/jcb.146.6.1227.
   PubMedGoogle Scholar
• Murai T, Nakase Y, Fukuda K, Chikashige Y, Tsutsumi C, Hiraoka Y, Matsumoto T. 2009. Distinctive responses to nitrogen starvation in the dominant active mutants of the fission yeast Rheb GTPase. Genetics 183:517–527. http://dx.doi.org/10.1534/genetics.109.105379.
   PubMedGoogle Scholar
• Kang SA, Pacold ME, Cervantes CL, Lim D, Lou HJ, Ottina K, Gray NS, Turk BE, Yaffe MB, Sabatini DM. 2013. mTORC1 phosphorylation sites encode their sensitivity to starvation and rapamycin. Science 341:1236566. http://dx.doi.org/10.1126/science.1236566.
   PubMed Web of Science ®Google Scholar
• Aspuria PJ, Sato T, Tamanoi F. 2007. The TSC/Rheb/TOR signaling pathway in fission yeast and mammalian cells: temperature sensitive and constitutive active mutants of TOR. Cell Cycle 6:1692–1695. http://dx.doi.org/10.4161/cc.6.14.4478.
   PubMed Web of Science ®Google Scholar
• Nakashima A, Sato T, Tamanoi F. 2010. Fission yeast TORC1 regulates phosphorylation of ribosomal S6 proteins in response to nutrients and its activity is inhibited by rapamycin. J. Cell Sci. 123:777–786. http://dx.doi.org/10.1242/jcs.060319.
   PubMed Web of Science ®Google Scholar
• Du W, Halova L, Kirkham S, Atkin J, Petersen J. 2012. TORC2 and the AGC kinase Gad8 regulate phosphorylation of the ribosomal protein S6 in fission yeast. Biol. Open 1:884–888. http://dx.doi.org/10.1242/bio.20122022.
   PubMedGoogle Scholar
• Ma N, Liu Q, Zhang L, Henske EP, Ma Y. 2013. TORC1 signaling is governed by two negative regulators in fission yeast. Genetics 195:457–468. http://dx.doi.org/10.1534/genetics.113.154674.
   PubMed Web of Science ®Google Scholar
• Aravind L, Koonin EV. 2001. The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol. 2(3):RESEARCH0007.1–0007.8. http://genomebiology.com/2001/2/3/research/0007 1.
   Google Scholar
• Korvald H, Molstad Moe AM, Cederkvist FH, Thiede B, Laerdahl JK, Bjoras M, Alseth I. 2011. Schizosaccharomyces pombe Ofd2 is a nuclear 2-oxoglutarate and iron dependent dioxygenase interacting with histones. PLoS One 6:e25188.
   PubMedGoogle Scholar
• Ikeda K, Morigasaki S, Tatebe H, Tamanoi F, Shiozaki K. 2008. Fission yeast TOR complex 2 activates the AGC-family Gad8 kinase essential for stress resistance and cell cycle control. Cell Cycle 7:358–364. http://dx.doi.org/10.4161/cc.7.3.5245.
   PubMed Web of Science ®Google Scholar
• Tatebe H, Morigasaki S, Murayama S, Zeng CT, Shiozaki K. 2010. Rab-family GTPase regulates TOR complex 2 signaling in fission yeast. Curr. Biol. 20:1975–1982. http://dx.doi.org/10.1016/j.cub.2010.10.026.
   PubMed Web of Science ®Google Scholar
• Iyer G, Hanrahan AJ, Milowsky MI, Al-Ahmadie H, Scott SN, Janakiraman M, Pirun M, Sander C, Socci ND, Ostrovnaya I, Viale A, Heguy A, Peng L, Chan TA, Bochner B, Bajorin DF, Berger MF, Taylor BS, Solit DB. 2012. Genome sequencing identifies a basis for everolimus sensitivity. Science 338:221. http://dx.doi.org/10.1126/science.1226344.
   PubMed Web of Science ®Google Scholar
• Loenarz C, Schofield CJ. 2008. Expanding chemical biology of 2-oxoglutarate oxygenases. Nat. Chem. Biol. 4:152–156. http://dx.doi.org/10.1038/nchembio0308-152.
   PubMed Web of Science ®Google Scholar
• Nakase Y, Nakase M, Kashiwazaki J, Murai T, Otsubo Y, Mabuchi I, Yamamoto M, Takegawa K, Matsumoto T. 2013. Fission yeast Any1, beta-arrestin-like protein, is involved in TSC-Rheb signaling and the regulation of amino acid transporters. J. Cell Sci. 126:3972–3981. http://dx.doi.org/10.1242/jcs.128355.
   PubMedGoogle Scholar
• Beck T, Hall MN. 1999. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402:689–692. http://dx.doi.org/10.1038/45287.
   PubMed Web of Science ®Google Scholar
• Yanagida M. 2009. Cellular quiescence: are controlling genes conserved? Trends Cell Biol. 19:705–715. http://dx.doi.org/10.1016/j.tcb.2009.09.006.
   PubMed Web of Science ®Google Scholar
• Muller I, Zimmermann M, Becker D, Flomer M. 1980. Calendar life span versus budding life span of Saccharomyces cerevisiae. Mech. Ageing Dev. 12:47–52. http://dx.doi.org/10.1016/0047-6374(80)90028-7.
   PubMed Web of Science ®Google Scholar
• Aris JP, Fishwick LK, Marraffini ML, Seo AY, Leeuwenburgh C, Dunn WAJr. 2012. Amino acid homeostasis and chronological longevity in Saccharomyces cerevisiae. Subcell. Biochem. 57:161–186. http://dx.doi.org/10.1007/978-94-007-2561-4_8.
   PubMedGoogle Scholar